{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T11:02:24Z","timestamp":1789988544658,"version":"4.0.1"},"reference-count":42,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T00:00:00Z","timestamp":1789948800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"},{"start":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T00:00:00Z","timestamp":1789948800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Insect Science"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Most insects protect their eggs from natural enemies via physical coverings, yet defensive mechanisms of exposed eggs (i.e., those without such coverings), particularly those lacking toxins, remain largely unexplored. The oak silkworm (\n                    <jats:italic>Antheraea pernyi<\/jats:italic>\n                    ) lays such exposed eggs, yet these eggs exhibit less parasitism than manually extracted washed eggs (MUWE) under laboratory conditions, raising the question of whether this defense operates in nature and how it functions. Here, field experiments showed that naturally laid unwashed eggs had significantly lower parasitism by three parasitoid species than MUWE. Behavioral parasitism assays showed the specialist\n                    <jats:italic>M. trabalae<\/jats:italic>\n                    nearly avoided intact naturally laid unwashed eggs (\u22642.5%), while generalist\n                    <jats:italic>A. japonicus<\/jats:italic>\n                    displayed fewer contacts and oviposition attempts. Y\u2010tube olfactometry verified egg\u2010derived volatiles mediate this repellency. Gas chromatography\u2212mass spectrometry analysis identified 2\u2010ethyl\u20101\u2010hexanol (2EH) as a key volatile unique to naturally laid eggs. Electroantennography confirmed dose\u2010dependent antennal responses to 2EH in both species. Y\u2010tube assays showed that 2EH repels\n                    <jats:italic>A. japonicus<\/jats:italic>\n                    at \u2265 5\n                    <jats:italic>\u00b5<\/jats:italic>\n                    g and\n                    <jats:italic>M. trabalae<\/jats:italic>\n                    at doses as low as 500 ng. Crucially, supplementing MUWE with 2EH greatly decreased the parasitism success in both parasitoids. This study reveals that egg\u2010associated 2EH acts as a chemical shield protecting exposed eggs from parasitoids, demonstrating that exposed eggs are not inherently vulnerable but rather employ volatile\u2010mediated defense against natural enemies. These findings advance our understanding of insect egg defense strategies, illuminate the evolutionary arms race between hosts and parasitoids, and establish a theoretical foundation for optimizing natural enemy mass rearing and developing behavioral regulators in biological control.\n                  <\/jats:p>","DOI":"10.1111\/1744-7917.70355","type":"journal-article","created":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T10:37:36Z","timestamp":1789987056000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Egg volatiles of oak silkworm mediate defense against parasitoid wasps"],"prefix":"10.1111","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5471-8179","authenticated-orcid":false,"given":"Hai\u2010Xia","family":"Zhan","sequence":"first","affiliation":[{"name":"State Key Laboratory of Green Pesticides Guizhou University  Guiyang China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Feng\u2010Qi","family":"Li","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Green Pesticides Guizhou University  Guiyang China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9313-0802","authenticated-orcid":false,"given":"Rui","family":"Tang","sequence":"additional","affiliation":[{"name":"Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology Guangdong Academy of Sciences  Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8334-3313","authenticated-orcid":false,"given":"Guy","family":"Smagghe","sequence":"additional","affiliation":[{"name":"Institute of Entomology Guizhou University  Guiyang China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haneef","family":"Tariq","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Green Pesticides Guizhou University  Guiyang China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Su","family":"Wang","sequence":"additional","affiliation":[{"name":"Institute of Plant Protection Beijing Academy of Agriculture and Forestry Sciences  Beijing China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9964-0512","authenticated-orcid":false,"given":"Lian\u2010Sheng","family":"Zang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Green Pesticides Guizhou University  Guiyang China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,9,21]]},"reference":[{"key":"e_1_2_7_2_1","doi-asserted-by":"crossref","first-page":"5417","DOI":"10.1016\/j.cub.2024.10.005","article-title":"The polyvalent sequestration ability of an economically important beetle","volume":"34","author":"Arce C.C.M.","year":"2024","journal-title":"Current Biology"},{"key":"e_1_2_7_3_1","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1007\/s10340-015-0681-z","article-title":"Invasion biology of spotted wing Drosophila suzukii: a global perspective and future priorities","volume":"88","author":"Asplen M.K.","year":"2015","journal-title":"Journal of Pest Science"},{"key":"e_1_2_7_4_1","doi-asserted-by":"crossref","first-page":"9029","DOI":"10.1073\/pnas.0402480101","article-title":"Plant\u2010derived pyrrolizidine alkaloid protects eggs of a moth (Utetheisa ornatrix) against a parasitoid wasp (Trichogramma ostriniae)","volume":"101","author":"Bezzerides A.","year":"2004","journal-title":"Proceedings of the National Academy of Sciences USA"},{"key":"e_1_2_7_5_1","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1007\/s10340-019-01155-z","article-title":"Host marking pheromone and GF120\u2122 applied in a push\u2010pull scheme reduce grapefruit infestation by Anastrepha ludens in field\u2010cage studies","volume":"93","author":"Birke A.","year":"2019","journal-title":"Journal of Pest Science"},{"key":"e_1_2_7_6_1","doi-asserted-by":"crossref","first-page":"854","DOI":"10.3390\/insects13090854","article-title":"Lymantria dispar (L.) (Lepidoptera: Erebidae): current status of biology, ecology, and management in Europe with notes from North America","volume":"13","author":"Boukouvala M.C.","year":"2022","journal-title":"Insects"},{"key":"e_1_2_7_7_1","doi-asserted-by":"crossref","first-page":"1789","DOI":"10.1002\/ps.6796","article-title":"Chinese oak silkworm Antheraea pernyi egg, a suitable factitious host for rearing eupelmid egg parasitoids","volume":"78","author":"Chen Y.M.","year":"2022","journal-title":"Pest Management Science"},{"key":"e_1_2_7_8_1","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1007\/s10340-020-01271-1","article-title":"Performances of six eupelmid egg parasitoids from China on Japanese giant silkworm Caligula japonica with different host age regimes","volume":"94","author":"Chen Y.M.","year":"2020","journal-title":"Journal of Pest Science"},{"key":"e_1_2_7_9_1","doi-asserted-by":"crossref","first-page":"9933","DOI":"10.1021\/acs.jafc.8b04481","article-title":"Identification of glutamic acid as a host marking pheromone of the African fruit fly species Ceratitis rosa (Diptera: Tephritidae)","volume":"66","author":"Cheseto X.","year":"2018","journal-title":"Journal of Agricultural and Food Chemistry"},{"key":"e_1_2_7_10_1","doi-asserted-by":"crossref","first-page":"1585","DOI":"10.1002\/ps.7331","article-title":"Field evaluation of glutathione and glutamic acid as host marking pheromones for control of tephritid fruit flies in a mango orchard in Kenya","volume":"79","author":"Cheseto X.","year":"2023","journal-title":"Pest Management Science"},{"key":"e_1_2_7_11_1","doi-asserted-by":"crossref","DOI":"10.5962\/bhl.title.82303","volume-title":"On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life","author":"Darwin C.","year":"1859"},{"key":"e_1_2_7_12_1","doi-asserted-by":"crossref","first-page":"1372","DOI":"10.1111\/1755-0998.13199","article-title":"A chromosome\u2010scale genome assembly of Antheraea pernyi (Saturniidae, Lepidoptera)","volume":"20","author":"Duan J.","year":"2020","journal-title":"Molecular Ecology Resources"},{"key":"e_1_2_7_13_1","doi-asserted-by":"crossref","first-page":"1634","DOI":"10.1073\/pnas.030532797","article-title":"Chemical defense against predation in an insect egg","volume":"97","author":"Eisner T.","year":"2000","journal-title":"Proceedings of the National Academy of Sciences USA"},{"key":"e_1_2_7_14_1","doi-asserted-by":"crossref","DOI":"10.1098\/rspb.2020.0344","article-title":"How to escape from insect egg parasitoids: a review of potential factors explaining parasitoid absence across the Insecta","volume":"287","author":"Fatouros N.E.","year":"2020","journal-title":"Proceedings of the Royal Society B: Biological Sciences"},{"key":"e_1_2_7_15_1","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1126\/science.abb6396","article-title":"Horizontally transmitted parasitoid killing factor shapes insect defense to parasitoids","volume":"373","author":"Gasmi L.","year":"2021","journal-title":"Science"},{"key":"e_1_2_7_16_1","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2215442119","article-title":"Sex pheromone communication in an insect parasitoid, Campoletis chlorideae Uchida","volume":"119","author":"Guo H.","year":"2020","journal-title":"Proceedings of the National Academy of Sciences USA"},{"key":"e_1_2_7_17_1","doi-asserted-by":"crossref","first-page":"8842","DOI":"10.1021\/acs.jafc.4c13266","article-title":"Megalurothrips usitatus feeding\u2010induced de novo synthesis of the C8 volatiles 1\u2010octen\u20103\u2010ol and 2\u2010ethyl\u20101\u2010hexanol in cowpea plants regulates plant\u2013herbivore\u2013predator interactions","volume":"73","author":"He Y.","year":"2025","journal-title":"Journal of Agricultural and Food Chemistry"},{"key":"e_1_2_7_18_1","doi-asserted-by":"crossref","DOI":"10.1002\/9780470760253","volume-title":"Chemoecology of Insect Eggs and Egg Deposition","author":"Hilker M.","year":"2003"},{"key":"e_1_2_7_19_1","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1146\/annurev-ento-120120-100746","article-title":"Adaptive plasticity of insect eggs in response to environmental challenges","volume":"68","author":"Hilker M.","year":"2023","journal-title":"Annual Review of Entomology"},{"key":"e_1_2_7_20_1","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1146\/annurev-ecolsys-110316-022628","article-title":"Apparent competition","volume":"48","author":"Holt R.D.","year":"2017","journal-title":"Annual Review of Ecology Evolution and Systematics"},{"key":"e_1_2_7_21_1","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1127\/entomologia\/2022\/1443","article-title":"Spodoptera frugiperda egg mass scale thickness modulates Trichogramma parasitoid performance","volume":"42","author":"Hou Y.Y.","year":"2022","journal-title":"Entomologia Generalis"},{"key":"e_1_2_7_22_1","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1146\/annurev.ento.48.091801.112733","article-title":"Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon","volume":"48","author":"Kennedy G.G.","year":"2003","journal-title":"Annual Review of Entomology"},{"key":"e_1_2_7_23_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.palaeo.2019.109337","article-title":"Earliest record of exophytic insect oviposition on plant material from the latest Pennsylvanian (Gzhelian, Stephanian C) of the Saale Basin, Germany","volume":"534","author":"Laa\u00df M.","year":"2019","journal-title":"Palaeogeography, Palaeoclimatology, Palaeoecology"},{"key":"e_1_2_7_24_1","doi-asserted-by":"crossref","first-page":"1345","DOI":"10.1007\/s10340-023-01639-z","article-title":"Current status of the biological control of the fall armyworm Spodoptera frugiperda by egg parasitoids","volume":"96","author":"Li T.H.","year":"2023","journal-title":"Journal of Pest Science"},{"key":"e_1_2_7_25_1","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1111\/brv.13130","article-title":"Egg coverings in insects: ecological adaptation to abiotic and biotic selective pressures","volume":"100","author":"Li T.H.","year":"2025","journal-title":"Biological Reviews"},{"key":"e_1_2_7_26_1","doi-asserted-by":"crossref","first-page":"1404","DOI":"10.1093\/jee\/tox140","article-title":"Antheraea pernyi (Lepidoptera: Saturniidae) and its importance in sericulture, food consumption, and traditional Chinese medicine","volume":"110","author":"Li W.","year":"2017","journal-title":"Journal of Economic Entomology"},{"key":"e_1_2_7_27_1","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1126\/science.ade5156","article-title":"Evolutionary transitions from camouflage to aposematism: hidden signals play a pivotal role","volume":"379","author":"Loeffler\u2010Henry K.","year":"2023","journal-title":"Science"},{"key":"e_1_2_7_28_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.celrep.2025.116035","article-title":"Piezo mediates oviposition in shielding gaps to protect moth eggs from parasitoid wasp","volume":"44","author":"Ma B.","year":"2025","journal-title":"Cell Reports"},{"key":"e_1_2_7_29_1","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1016\/j.cub.2012.01.045","article-title":"Alcohol consumption as self\u2010medication against blood\u2010borne parasites in the fruit fly","volume":"22","author":"Milan N.F.","year":"2012","journal-title":"Current Biology"},{"key":"e_1_2_7_30_1","doi-asserted-by":"crossref","first-page":"4476","DOI":"10.1038\/s41467-022-32203-5","article-title":"Search performance and octopamine neuronal signaling mediate parasitoid induced changes in Drosophila oviposition behavior","volume":"13","author":"Pang L.","year":"2022","journal-title":"Nature Communications"},{"key":"e_1_2_7_31_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.biocontrol.2019.104100","article-title":"Attraction of Chelonus insularis to host and host habitat volatiles during the search of Spodoptera frugiperda eggs","volume":"140","author":"Roque\u2010Romero L.","year":"2020","journal-title":"Biological Control"},{"key":"e_1_2_7_32_1","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1146\/annurev.ento.50.071803.130420","article-title":"Evolutionary ecology of insect immune defenses","volume":"50","author":"Schmid\u2010Hempel P.","year":"2005","journal-title":"Annual Review of Entomology"},{"key":"e_1_2_7_33_1","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1017\/S000748532000019X","article-title":"Kairomones from Euschistus heros egg masses and their potential use for Telenomus podisi parasitism improvement","volume":"110","author":"Tognon R.","year":"2020","journal-title":"Bulletin of Entomological Research"},{"key":"e_1_2_7_34_1","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.1007\/s10886-016-0754-3","article-title":"Volatiles mediating parasitism of Euschistus conspersus and Halyomorpha halys eggs by Telenomus podisi and Trissolcus erugatus","volume":"42","author":"Tognon R.","year":"2016","journal-title":"Journal of Chemical Ecology"},{"key":"e_1_2_7_35_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1146\/annurev-ento-021622-111028","article-title":"Complex and beautiful: unraveling the intricate communication systems among plants and insects","volume":"68","author":"Tumlinson J.H.","year":"2023","journal-title":"Annual Review of Entomology"},{"key":"e_1_2_7_36_1","doi-asserted-by":"crossref","first-page":"4237","DOI":"10.1038\/s41467-019-12175-9","article-title":"A chromosome\u2010level genome assembly provides insights into chemical ecology and insecticide resistance","volume":"10","author":"Wan F.H.","year":"2019","journal-title":"Nature Communications"},{"key":"e_1_2_7_37_1","doi-asserted-by":"crossref","first-page":"694","DOI":"10.3390\/insects12080694","article-title":"Parasitism and suitability of Aprostocetus brevipedicellus on Chinese oak silkworm, Antheraea pernyi, a dominant factitious host","volume":"12","author":"Wang J.","year":"2021","journal-title":"Insects"},{"key":"e_1_2_7_38_1","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1127\/entomologia\/2020\/1060","article-title":"Manually\u2010extracted unfertilized eggs of Chinese oak silkworm, Antheraea pernyi, enhance mass production of Trichogramma parasitoids","volume":"40","author":"Wang Y.","year":"2020","journal-title":"Entomologia Generalis"},{"key":"e_1_2_7_39_1","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1038\/nature25479","article-title":"Biomechanics of predator\u2013prey arms race in lion, zebra, cheetah and impala","volume":"554","author":"Wilson A.M.","year":"2018","journal-title":"Nature"},{"key":"e_1_2_7_40_1","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1146\/annurev-ento-060120-091620","article-title":"Biological control with Trichogramma in China: history, present status, and perspectives","volume":"66","author":"Zang L.S.","year":"2021","journal-title":"Annual Review of Entomology"},{"key":"e_1_2_7_41_1","doi-asserted-by":"crossref","first-page":"12820","DOI":"10.1021\/acs.jafc.6c01693","article-title":"Identification of odorant\u2010binding protein AjapOBP26 as the key mediator of 2\u2010ethyl\u20101\u2010hexanol avoidance in the egg parasitoid Anastatus japonicus","volume":"74","author":"Zhan H.X.","year":"2026","journal-title":"Journal of Agricultural and Food Chemistry"},{"key":"e_1_2_7_42_1","doi-asserted-by":"publisher","DOI":"10.1111\/1744\u20107917.70268"},{"key":"e_1_2_7_43_1","doi-asserted-by":"crossref","first-page":"915","DOI":"10.3390\/plants12040915","article-title":"Identification and comparative expression profiles of candidate olfactory receptors in the transcriptomes of the important egg parasitoid wasp Anastatus japonicus Ashmead (Hymenoptera: Eupelmidae)","volume":"12","author":"Zhan H.X.","year":"2023","journal-title":"Plants"}],"container-title":["Insect Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/1744-7917.70355","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/1744-7917.70355","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/1744-7917.70355","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T10:37:42Z","timestamp":1789987062000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/1744-7917.70355"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,21]]},"references-count":42,"alternative-id":["10.1111\/1744-7917.70355"],"URL":"https:\/\/doi.org\/10.1111\/1744-7917.70355","archive":["Portico"],"relation":{},"ISSN":["1672-9609","1744-7917"],"issn-type":[{"value":"1672-9609","type":"print"},{"value":"1744-7917","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,21]]},"assertion":[{"value":"2026-03-26","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-08-19","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-21","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"1744-7917.70355"}}